Blood meal digestion and changes in lipid reserves are associated with the post-ecdysis development of the flight muscle and ovary in young adults of Rhodnius prolixus

Insects are widely spread in terrestrial environments and their exoskeleton, also named cuticle, has an important role in this success, since it serves as a protection against desiccation and mechanical injury. However, it limits insect size and growth, and thus, in order to grow in volume and undergo changes to reach adulthood, insects need to synthesize a new cuticle and shed the old one, a process called ecdysis. The periods between two sequential ecdyses are called instars and they are the immature stages in the insect life cycle (Esperk et al., 2007). Another key feature that contributed to insect prosperity evolved millions of years ago as they developed the powered flight, which allowed them to exploit new niches (Iwamoto, 2011). But only the adult stages possess functional wings, and to reach adulthood the insects must undergo metamorphosis (Truman, 2019), a process that happens after a series of ecdyses.

After the metamorphosis in Drosophila melanogaster, a holometabolous insect, the lipids play an important role in the success of the adults, as they are used to synthesize hydrocarbons, important to waterproof the cuticle and make the insect more resistant to dryness (Storelli et al., 2019). Besides cuticle impermeabilization, lipids have an essential role in the life of insects in general, as they are used for many metabolic functions such as growth, flight, embryo nutrition, survival to starvation, among other functions (Gondim et al., 2018, Toprak et al., 2020). The fat body plays a central role in lipid storage and mobilization as it is the main site of lipid synthesis and accumulation, and it is also the organ responsible for the synthesis of lipophorin (Lp), the lipoprotein present in insect hemolymph that is responsible for delivering the lipids to specific organs (Canavoso et al., 2001, Skowronek et al., 2021).

In the fat body, neutral lipids, mostly as triacylglycerol (TG), are stored in lipid droplets (LDs), which are cellular organelles consisting of a neutral lipid core, surrounded by a phospholipid monolayer which contains diverse associated proteins (Toprak et al., 2020; Walther and Farese, 2012). When lipids are abundant, their content in the LDs increase, and they are mobilized when required, as during starvation. TG synthesis depends on the availability of fatty acids, which are either directly acquired from the diet or synthesized de novo from other substrates. Insects with different feeding habits may synthesize lipids de novo, using acetyl-CoA derived from ingested carbohydrates and/or amino acids, and lipogenesis de novo has been shown to importantly contribute to lipid accumulation in various insect species, as D. melanogaster, Aedes aegypti and Rhodnius prolixus (Alabaster et al., 2011, Moraes et al., 2022, Saraiva et al., 2021, Wicker-Thomas et al., 2015).

R. prolixus, a hemimetabolous insect, is an important vector of Chagas disease in South and Central Americas (de Fuentes-Vicente et al., 2018). It is an obligatory hematophagous insect during the entire life cycle, nymphs and adults and, after a blood meal, the adults accumulate TG in the fat body which is mobilized later on, during starvation (Pontes et al, 2008). These lipids can be synthesized de novo by the fat body, from amino acids obtained from the blood meal, and can also be directly obtained from the ingested blood, transported in the hemolymph by Lp (Grillo et al., 2007, Saraiva et al., 2021).

The flight muscle of R. prolixus is known to have a large amount of TG stored in LDs (Ward et al., 1982); however, the moment in which this accumulation occurs has not been determined yet. Moreover, it is not clear what are the roles of these lipids found in the flight muscle; it is believed that they serve as fuel for flight, but whether this is their only role is still to be investigated (Oliveira et al., 2006). When the mitochondrial β-oxidation was impaired in R. prolixus adult females during starvation, after the knockdown of the mitochondrial trifunctional protein A subunit (HADHA), TG accumulated in the fat body and the insect’s ability to fly diminished (Arêdes et al., 2022). In the cricket Gryllus bimaculatus it was shown that lipids and carbohydrates from the flight muscle play a role in improving oviposition of female crickets (Lorenz, 2007). The tsetse fly, Glossina morsitans, uses amino acids, especially alanine, and lipids from the fat body to produce proline which then reaches the flight muscle to fuel flight (Bursell, 1977), showing that lipid utilization by the flight muscle can be indirect, through a cyclic relationship with the fat body.

Herein, we have investigated the moment when lipid accumulation in the flight muscle occurs in R. prolixus life cycle. In our colony, after insects’ molt from fifth instar nymphs to adults (around 15 – 20 days after feeding), it takes two – three more weeks before these insects are fed the first time as adults, because it has been observed that a few days after molting the adults are still not willing to ingest blood. Thus, we have followed the first fifteen days of the insect as an adult, to track lipid deposition in the flight muscle. We report changes in the protein and TG contents of R. prolixus’ organs in the days following its final molt, and show that the flight muscle undergoes drastic changes in its size, as well as in its LD pattern, which indicated that a maturation process took place, with relevant physiological differences between the insect first days after molting and its further adult form.

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